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WRKY transcription factors (TFs) play an important role in plant responses to biotic and abiotic stress as well as in plant growth and development. In the present study, bioinformatics methods were used to identify members of the WRKY transcription factor family in the <i>Musa acuminata</i> (DH-Pahang) genome (version 2). A total of 164 <i>MaWRKY</i><i>s</i> were identified and phylogenetic analysis showed that MaWRKYs could be categorized into three subfamilies. Overall, the 162 <i>MaWRKYs</i> were distributed on 11 chromosomes, and 2 genes were not located on the chromosome. There were 31 collinear genes from segmental duplication and 7 pairs of genes from tandem duplication. RNA-sequencing was used to analyze the expression profiles of <i>MaWRKYs</i> in different fruit development, ripening stages, under various abiotic and biotic stressors. Most of the <i>MaWRKY</i><i>s</i> showed a variety of expression patterns in the banana fruit development and ripening stages. Some <i>MaWRKYs</i> responded to abiotic stress, such as low temperature, drought, and salt stress. Most differentially expressed <i>MaWRKYs</i> were downregulated during banana’s response to Foc TR4 infection, which plays an important role in physiological regulation to stress. Our findings indicate that <i>MaWRKY21</i> directly binds to the W-box of the <i>MaICS</i> promoter to decrease <i>MaICS</i> transcription and then reduce the enzyme activity. These studies have improved our understanding of the molecular basis for the development and stress resistance of an important banana variety.